Katalin M Gothard
The majority of neurophysiological studies that have explored the role of the primate amygdala in the evaluation of social signals have relied on visual stimuli such as images of facial expressions. Vision, however, is not the only sensory modality that carries social signals. Both humans and nonhuman primates exchange emotionally meaningful social signals through touch. Indeed, social grooming in nonhuman primates and caressing touch in humans is critical for building lasting and reassuring social bonds. To determine the role of the amygdala in processing touch, we recorded the responses of single neurons in the macaque amygdala while we applied tactile stimuli to the face. We found that one-third of the recorded neurons responded to tactile stimulation. Although we recorded exclusively from the right amygdala, the receptive fields of 98% of the neurons were bilateral. A fraction of these tactile neurons were monitored during the production of facial expressions and during facial movements elicited occasionally by touch stimuli. Firing rates arising during the production of facial expressions were similar to those elicited by tactile stimulation. In a subset of cells, combining tactile stimulation with facial movement further augmented the firing rates. This suggests that tactile neurons in the amygdala receive input from skin mechanoceptors that are activated by touch and by compressions and stretches of the facial skin during the contraction of the underlying muscles. Tactile neurons in the amygdala may play a role in extracting the valence of touch stimuli and/or monitoring the facial expressions of self during social interactions.
Videos with rich social and emotional content elicit natural social behaviors in primates. Indeed, while watching videos of conspecifics, monkeys engage in eye contact, gaze follow, and reciprocate facial expressions. We hypothesized that the frequency and timing of eyeblinks also depends on the social signals contained in videos. We monitored the eyeblinks of four male adult macaques while they watched videos of conspecifics displaying facial expressions with direct or averted gaze. The instantaneous blink rate of all four animals decreased during videos. The temporal synchrony of blinking, however, increased in response to segments depicting appeasing or aggressive facial expressions directed at the viewer. Two of the four monkeys, who systematically reciprocated the direct gaze of the stimulus monkeys, also showed eyeblink entrainment, a temporal coordination of blinking between social partners engaged in dyadic interactions. Together, our results suggest that in macaques, as in humans, blinking depends not only on the physiological imperative to protect the eyes and spread a film of tears over the cornea, but also on several socio-emotional factors.